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Rabies Genetic Diversity and Reservoir Identification in Terrestrial Carnivores

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Rabies Genetic Diversity and Reservoir Identification in Terrestrial Carnivores Rabies Genetic Diversity and Reservoir Identification in Terrestrial Carnivores Throughout Ethiopia DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Laura Elyse Binkley Graduate Program in Comparative and Veterinary Medicine The Ohio State University 2019 Dissertation Committee: Wondwossen A. Gebreyes, Advisor Jeanette O’Quin, Co-advisor Laura Pomeroy Andrés Velasco-Villa Robert J. Gates Michael S. Bisesi Copyrighted by Laura Elyse Binkley 2019 Abstract Ethiopia has long been among the most rabies-affected countries in the world with an annual incidence rate of 1.6/100,000 population. Domestic dogs serve as the principal reservoir for rabies transmission however, little information exists regarding the genetic diversity of RABVs circulating in dogs or the existence of cycles maintained by other mammalian species. Identifying all reservoirs of rabies plays a crucial role in effective disease control. Objectives include 1.) Investigation of the genetic diversity of rabies circulating in wild and domestic species throughout Ethiopia; 2.) Identification of intraspecies and interspecies contact rates at communal foraging sites; 3.) Application of contact rate estimates to mathematical expressions that will help determine maintenance potential. This work comprises the study of 230 partial and complete N-gene sequences obtained from both wild and domestic species collected throughout different regions of Ethiopia during the period 2010-2017. Camera traps were used to examine contact rates within and between terrestrial carnivore species at communal foraging sites. These contact rates were then applied to expressions of the basic reproductive number to determine the rabies maintenance potential of populations. Results identified the existence of a major dog rabies epizootic throughout Ethiopia involving a homogeneous RABV variant that has been spreading from an ii epicenter in the Oromia region. Additionally, a 3.3% divergent RABV variant circulating in side-stripped jackals was identified. Intraspecies contact rates and calculations of maintenance potential were highest in domestic dogs followed by spotted hyenas and domestic cats, respectively. Interspecies contact rates and calculations of maintenance potential were highest between domestic cats and spotted hyenas. This snapshot of rabies dynamics in Ethiopia provides important baseline data for prevention and control efforts and serves as the first steps in identifying wildlife reservoir hosts for rabies transmission throughout the country. iii Acknowledgments The Acknowledgments page is optional. This page includes a brief, sincere, professional acknowledgment of the assistance received from individuals, advisor, faculty, and institution. iv Vita 2005................................................................Bishop Watterson High School 2009................................................................B.A. Zoology, Ohio Wesleyan University 2014................................................................M.P.H. Environmental Public Health, Veterinary Public Health, The Ohio State University 2015................................................................M.S. Environment and Natural Resources, The Ohio State University 2015 to present ..............................................Graduate Research Associate, Department of Veterinary Preventive Medicine, The Ohio State University Publications Cunningham, D., DeBarber, A.E., Bir, N., Binkley. L., Merkens, L.S., Steiner, R.D., and Herman, G.E. 2015. Analysis of Hedgehog Signaling in Cerebellar Granule Cell Precursors in a Conditional Nsdhl Allele Demonstrates an Essential Role for v Cholesterol in Postnatal CNS Development. Human Molecular Genetics. doi:10.1093/hmg/ddv042. Fields of Study Major Field: Comparative and Veterinary Medicine vi Table of Contents Abstract ............................................................................................................................... ii Acknowledgments.............................................................................................................. iv Vita ...................................................................................................................................... v Publications ......................................................................................................................... v Fields of Study ................................................................................................................... vi Table of Contents .............................................................................................................. vii List of Tables ................................................................................................................... xiii List of Figures .................................................................................................................. xvi Chapter 1: Introduction ...................................................................................................... 1 Chapter 2: Literature Review .............................................................................................. 8 Emerging Diseases from Wildlife: .................................................................................. 8 Virology and General Molecular Epidemiology of the Rabies Virus: .......................... 17 Basic Virology ........................................................................................................... 17 Rabies Virus Life Cycle ............................................................................................ 20 Transmission, Pathogenesis and Treatment ............................................................... 23 vii Molecular Methods for Identification of Rabies Virus and Distinguishing Variants 26 Rabies Virus Phylogeny in Africa ............................................................................. 43 Phylogenetic Analysis Summary and Applications................................................... 45 Ethiopia as a Hotspot for Emerging Infectious Disease:............................................... 47 Effects of Biodiversity on Infectious Disease ........................................................... 47 Ethiopia as a Hotspot ................................................................................................. 51 Basics of Rabies in Ethiopia: ........................................................................................ 54 Modeling Basics and Obtaining Modeling Data from Wildlife: ................................... 58 The Model-Based Approach ...................................................................................... 58 Modeling Basics ........................................................................................................ 60 Allometrics as a Means to Simplify Parameterization .............................................. 72 Who Acquires Infection from Whom (WAIFW) Matrix Model ............................... 74 Additional Methods to Consider When Examining Host-Species Heterogeneity in a Multi-Host System According to Streicker et al. 2014 ............................................. 79 Network Models for Wildlife According to Craft and Caillaud 2011 ....................... 81 Obtaining Modeling Data from Wildlife ................................................................... 82 Multi-Species Infectious Disease Models for Wildlife Populations: ............................ 87 Key Definitions.......................................................................................................... 87 The Reservoir ............................................................................................................ 89 viii Management Methods and when to Target the Reservoir ......................................... 91 Framework of Basic Theoretical Transmission Pathway Models ............................. 92 Sources of Variation within the Continuum/ Stochasticity ....................................... 99 The Stochastic Model and Comparison ................................................................... 101 Continuum Updated and Re-Explained ................................................................... 103 Methods Used to Identify Reservoirs and Establish Transmission Dynamics ........ 107 Existing Scenario in the Serengeti Ecosystem: ........................................................... 113 Reservoir Identification and Multi-Species Pathogen Study Designs ..................... 113 Spatial Models for Multi-Species Pathogen ............................................................ 123 Network Models to Examine Within-and-Between Species Transmission Rates ... 126 Spotted Hyenas of the Serengeti: Asymptomatic Rabies Carrier Theory and Transmission Parameters ......................................................................................... 130 Rabies Transmission in Southern Africa and Kenya: ................................................. 134 Background .............................................................................................................. 134 Mongoose Rabies .................................................................................................... 137 Rabies in Wild Canids of South Africa: Black-Backed Jackal (Canis mesomelas) and Bat- Eared Fox (Otocyon megalotis) ....................................................................... 143 Jackal Rabies
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